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Metagenomic Analysis Reveals Large Potential for Carbon, Nitrogen and Sulfur Cycling in Coastal Methanic Sediments of the Bothnian Sea

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Metagenomic Analysis Reveals Large Potential for Carbon, Nitrogen and Sulfur Cycling in Coastal Methanic Sediments of the Bothnian Sea bioRxiv preprint doi: https://doi.org/10.1101/553131; this version posted February 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Metagenomic analysis reveals large potential for carbon, nitrogen and sulfur cycling in coastal methanic sediments of the Bothnian Sea Olivia Rasigraf1,2,*,§, Niels A.G.M. van Helmond3, Jeroen Frank1,4, Wytze K. Lenstra3, Matthias Egger3,#, Caroline P. Slomp2,3, Mike S.M. Jetten1,2,4 1 Department of Microbiology, Radboud University Nijmegen, Nijmegen, The Netherlands 2 Netherlands Earth System Science Centre (NESSC), Utrecht, The Netherlands 3 Department of Earth Sciences, Utrecht University, The Netherlands 4 Soehngen Institute of Anaerobic Microbiology (SIAM), Radboud University Nijmegen, Nijmegen, The Netherlands *current address: German Research Centre for Geosciences (GFZ), Section 3.7 Geomicrobiology, Potsdam, Germany #current address: The Ocean Cleanup, Rotterdam, The Netherlands §corresponding author: [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/553131; this version posted February 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Abstract 2 3 The Bothnian Sea is an oligotrophic brackish basin characterized by low salinity and high 4 concentrations of reactive iron, methane and ammonium in the sediments potentially enabling an 5 intricate microbial network. Therefore, we analyzed and compared biogeochemical and microbial 6 profiles at one offshore and two near coastal sites in the Bothnian Sea. 16S rRNA amplicon 7 sequence analysis revealed stratification of both bacterial and archaeal taxa in accordance with 8 the geochemical gradients of iron, sulfate and methane. The communities at the two near coastal 9 sites were more similar to each other than that at the offshore site located at a greater water depth. 10 To obtain insights into the metabolic networks within the iron-rich methanic sediment layer 11 located below the sulfate-methane transition zone (SMTZ), we performed metagenomic 12 sequencing of sediment-derived DNA. Genome bins retrieved from the most abundant bacterial 13 and archaeal community members revealed a broad potential for respiratory sulfur metabolism 14 via partially reduced sulfur species. Nitrogen cycling was dominated by reductive processes via a 15 truncated denitrification pathway encoded exclusively by bacterial lineages. Gene-centric 16 fermentative metabolism analysis indicated the central role of acetate, formate, alcohols and 17 hydrogen in the analyzed anaerobic sediment. Methanogenic/-trophic pathways were dominated 18 by Methanosaetaceae, Methanosarcinaceae, Methanomassiliicoccaceae, Methanoregulaceae and 19 ANME-2 archaea. Thorarchaeota and Bathyarchaeota encoded pathways for acetogenesis. Our 20 results indicate flexible metabolic capabilities of core community bacterial and archaeal taxa, 21 which can adapt to changing redox conditions, and with a spatial distribution in Bothnian Sea 22 sediments that is likely governed by the quality of available organic substrates. 23 2 bioRxiv preprint doi: https://doi.org/10.1101/553131; this version posted February 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 24 Introduction 25 26 Sediment microbial communities drive biogeochemical cycles through their specific metabolic 27 activities. The supply of organic carbon from primary production or terrestrial input via rivers, - 2- 28 and electron acceptors such as nitrate (NO3 ) and sulfate (SO4 ) in marine systems, will select for 29 particular microbial guilds. Together they will determine the establishment of environment- 30 specific metabolic networks and geochemical profiles. Despite the critical role of coastal 31 sediments in global biogeochemical cycling, for example, as a source of methane (CH4) (Bange 32 et al. 1994) and sink for nutrients (Asmala et al. 2017), our understanding of their microbial 33 community composition and how this is linked to the cycling of sulfur (S), carbon (C) and 34 nitrogen (N), is still incomplete. 35 The Bothnian Sea, a brackish basin located in the northern part of the Baltic Sea, is an ideal 36 location to study the linkage between microbes and biogeochemistry because of the distinct sharp 37 redox zonation of its surface sediments (Egger et al. 2015a; Lenstra et al. 2018; Rasigraf et al. 38 2017). The Bothnian Sea is oligotrophic and most organic matter in the sediment is supplied 2- 39 through rivers and is thus of terrestrial origin (Algesten et al. 2006). SO4 concentrations in the 2- 40 bottom water are low (3-5 mM), which has allowed the development of a relatively shallow SO4 41 reduction zone in the sediment at sites with relatively high sedimentation rates. At such sites, CH4 2- 42 is abundant in the lower part of the SO4 reduction zone, and a distinct sulfate-methane transition 43 zone (SMTZ) has developed (Egger et al. 2015a; Lenstra et al. 2018). The exact position of the 44 SMTZ varies with space and time depending on the sedimentation rate and the input of organic 45 matter (Egger et al. 2015a; Lenstra et al. 2018; Rooze et al. 2016; Slomp et al. 2013). The input 46 of reactive iron (oxyhydroxides, henceforth termed Fe oxides) is in general higher than sulfide 3 bioRxiv preprint doi: https://doi.org/10.1101/553131; this version posted February 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 47 (H2S) formation in the sediment resulting in net burial of Fe oxides below the SMTZ. Both 48 modeling and incubation studies suggest CH4 oxidation with Fe oxides as the electron acceptor in 2- 49 the SO4 -depleted methanic layers below the SMTZ (Egger et al. 2015b; Rooze et al. 2016; 50 Slomp et al. 2013). So far, the underlying pathways and responsible organisms for this process 51 are largely unknown. 52 Several studies have investigated the microbial community composition in sediments of the 53 Bothnian Bay and North Sea with 16S rRNA pyrosequencing techniques and speculated on 54 possible microbial guilds involved in CH4 and Fe cycling (Oni et al. 2015a; Reyes et al. 2016). In 55 surface sediments from the Skagerrak and Bothnian Bay, various potential Fe-reducers belonging 56 to Desulfobulbaceae, Desulfuromonadaceae and Pelobacteraceae families were identified 57 (Reyes et al. 2016). In deeper methanic sediment layers of the Helgoland area in the North Sea, 58 microbial populations predicted to be involved in Fe and CH4 cycling included uncultured 59 lineages of candidate division JS1 and methanogenic/-trophic archaea belonging to 60 Methanohalobium, Methanosaeta and anaerobic methane oxidizing archaea clade 3 (ANME-3) 61 (Oni et al. 2015a). Moreover, recent findings indicate that temperature is another factor which 62 can influence the pathway of crystalline Fe utilization in these sediments (Aromokeye et al. 63 2018). Investigations of microbial communities involved in Fe cycling are challenging due to the 64 absence of suitable ‘universal’ biomarkers. Different microbial groups have evolved different 65 mechanisms and underlying genes encoding responsible enzymes may be unrelated. Novel 66 mechanisms with unknown enzymatic steps in Fe reduction may exist but would remain 67 undetected. 68 Activity measurements and functional biomarker analysis showed the presence of various 69 pathways for N cycling in the Bothnian Sea and Bothnian Bay sediments (Bonaglia et al. 2017; 4 bioRxiv preprint doi: https://doi.org/10.1101/553131; this version posted February 18, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 70 Hellemann et al. 2017; Rasigraf et al. 2017; Reyes et al. 2017). Thus, for example, dissimilatory 71 nitrate reduction to ammonium (DNRA) and denitrification were shown to be of nearly equal 72 importance in oligotrophic sediments at a coastal site in the Bothnian Bay (Bonaglia et al. 2017). 73 These results contradict the common assumption that DNRA is of minor importance in 74 oligotrophic sediments with low organic carbon input and low rates of H2S production. Also, a 75 gene-centric approach for N-cycle potential was applied previously to the Bothnian Sea and 76 Bothnian Bay sediments. Sediment from the surface layer, SMTZ and deep methanic zone were 77 analyzed and showed that N cycling genes were most abundant in the surface layer with 78 denitrification being potentially the dominant pathway for N loss (Rasigraf et al. 2017). 79 Furthermore, in suboxic sediments from the Bothnian Bay, the genetic potential for 80 denitrification was far greater than that for DNRA (Reyes et al. 2017). With respect to the 81 nitrification potential, differences were found between analyzed sites in the Bothnian Sea and 82 Bothnian Bay. While in the central part of the Bothnian Sea, the nitrification potential was almost 83 exclusively attributed to ammonia oxidizing archaea (AOA) belonging to Thaumarchaeota 84 Marine Group-I (MG-I) (Rasigraf et al. 2017), in suboxic coastal sediments in the Bothnian Bay, 85 both AOA and ammonia oxidizing bacteria (AOB) seemed equally important (Reyes et al. 2017).
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